Skip to main content Accessibility help

An agent-based model of exposure to human toxocariasis: a multi-country validation

  • K. KANOBANA (a1), B. DEVLEESSCHAUWER (a2) (a3), K. POLMAN (a1) and N. SPEYBROECK (a3)


Seroprevalence data illustrate that human exposure to Toxocara is frequent. Environmental contamination with Toxocara spp. eggs is assumed to be the best indicator of human exposure, but increased risk of exposure has also been associated with many other factors. Reported associations are inconsistent, however, and there is still ambiguity regarding the factors driving the onset of Toxocara antibody positivity. The objective of this work was to assess the validity of our current conceptual understanding of the key processes driving human exposure to Toxocara. We constructed an agent-based model predicting Toxocara antibody positivity (as a measure of exposure) in children. Exposure was assumed to depend on the joint probability of 3 parameters: (1) environmental contamination with Toxocara spp. eggs, (2) larvation of these eggs and (3) the age-related contact with these eggs. This joint probability was linked to processes of acquired humoral immunity, influencing the rate of antibody seroreversion. The results of the simulation were validated against published data from 5 different geographical settings. Using simple rules and a stochastic approach with parameter estimates derived from the respective contexts, plausible serological patterns emerged from the model in nearly all settings. Our approach leads to novel insights in the transmission dynamics of Toxocara.


Corresponding author

*Corresponding author. Department of Biomedical Sciences, Unit of Medical Helminthology, Institute of Tropical Medicine, Nationalestraat 155, 2000 Antwerp, Belgium. E-mail:


Hide All
Alonso, J. M., Bojanich, M. V., Chamorro, M. and Gorodner, J. O. (2000). Toxocara seroprevalence in children from a subtropical city in Argentina. Revista do Instituto de Medicina Tropical de Sao Paulo 42, 235237. pii: S0036-46652000000400010.
Alonso, J. M., Stein, M., Chamorro, M. C. and Bojanich, M. V. (2001). Contamination of soils with eggs of Toxocara in a subtropical city in Argentina. Journal of Helminthology 75, 165168. pii: S0022149X01000245.
Altcheh, J., Nallar, M., Conca, M., Biancardi, M. and Freilij, H. (2003). Toxocariasis: clinical and laboratory features in 54 patients. Anales de pediatria (Barcelona, Spain: 2003) 58, 425431. pii: 13046522.
Anaruma, F. F., Chieffi, P. P., Correa, C. R., Camargo, E. D., Silveira, E. P., Aranha, J. J. and Ribeiro, M. C. (2002). Human toxocariasis: a seroepidemiological survey in the municipality of Campinas (SP), Brazil. Revista do Instituto de Medicina Tropical de Sao Paulo 44, 303307. pii: S0036-46652002000600002.
Avcioglu, H., Soykan, E. and Tarakci, U. (2011). Control of helminth contamination of raw vegetables by washing. Vector Borne and Zoonotic Diseases 11, 189191. doi: 10.1089/vbz.2009.0243.
Baboolal, S. and Rawlins, S. C. (2002). Seroprevalence of toxocariasis in schoolchildren in Trinidad. Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 139143.
Beaver, P. C., Snyder, C. H., Carrera, G. M., Dent, J. H. and Lafferty, J. W. (1952). Chronic eosinophilia due to visceral larva migrans; report of three cases. Pediatrics 9, 719.
Bonabeau, E. (1997). From classical models of morphogenesis to agent-based models of pattern formation. Artificial Life 3, 191211.
Buijs, J. and van, K. F. (1994). Toxocara infection in children and the relation with allergic manifestations. Veterinary Quarterly 16 (Suppl. 1), 13S14S.
Buijs, J., Borsboom, G., van Gemund, J. J., Hazebroek, A., van Dongen, P. A., van, K. F. and Neijens, H. J. (1994). Toxocara seroprevalence in 5-year-old elementary schoolchildren: relation with allergic asthma. American Journal of Epidemiology 140, 839847.
Buijs, J., Borsboom, G., Renting, M., Hilgersom, W. J., van Wieringen, J. C., Jansen, G. and Neijens, J. (1997). Relationship between allergic manifestations and Toxocara seropositivity: a cross-sectional study among elementary school children. European Respiratory Journal 10, 14671475.
Bwalya, E. C., Nalubamba, K. S., Hankanga, C. and Namangala, B. (2011). Prevalence of canine gastrointestinal helminths in urban Lusaka and rural Katete Districts of Zambia. Preventive Veterinary Medicine 100, 252255. pii: S0167-5877(11)00143-7; doi: 10.1016/j.prevetmed.2011.04.015.
Cilla, G., Perez-Trallero, E., Gutierrez, C., Part, C. and Gomariz, M. (1996). Seroprevalence of Toxocara infection in middle-class and disadvantaged children in northern Spain (Gipuzkoa, Basque Country). European Journal of Epidemiology 12, 541543.
Colli, C. M., Rubinsky-Elefant, G., Paludo, M. L., Falavigna, D. L., Guilherme, E. V., Mattia, S., Araujo, S. M., Ferreira, E. C., Previdelli, I. T. and Falavigna-Guilherme, A. L. (2010). Serological, clinical and epidemiological evaluation of toxocariasis in urban areas of south Brazil. Revista do Instituto de Medicina Tropical de Sao Paulo 52, 6974. pii: S0036-46652010000200002.
Congdon, P. and Lloyd, P. (2011). Toxocara infection in the United States: the relevance of poverty, geography and demography as risk factors, and implications for estimating county prevalence. International Journal of Public Health 56, 1524. doi: 10.1007/s00038-010-0143-6.
de Melker, H. E., van der Peet, T. E., Berbers, G. A., van de Akker, R., van Knapen, F., Schellekens, J. F. and Conyn-van Spaendonck, M. A. (1995). Pilot-onderzoek voor het Pienter-Project. Seroprevalenties voor bof, mazelen, rubella, kinkhoest, Toxoplasma gondii, Toxocara, T. spiralis an hepatitis A. 213675004. RIVM, Bilthoven, the Netherlands.
Elefant, G. R., Shimizu, S. H., Sanchez, M. C., Jacob, C. M. and Ferreira, A. W. (2006). A serological follow-up of toxocariasis patients after chemotherapy based on the detection of IgG, IgA, and IgE antibodies by enzyme-linked immunosorbent assay. Journal of Clinical Laboratory Analysis 20, 164172. doi: 10.1002/jcla.20126.
Fahrion, A. S., Staebler, S. and Deplazes, P. (2008). Patent Toxocara canis infections in previously exposed and in helminth-free dogs after infection with low numbers of embryonated eggs. Veterinary Parasitology 152, 108115. pii: S0304-4017(07)00632-2; doi: 10.1016/j.vetpar.2007.11.022.
Fontanarrosa, M. F., Vezzani, D., Basabe, J. and Eiras, D. F. (2006). An epidemiological study of gastrointestinal parasites of dogs from Southern Greater Buenos Aires (Argentina): age, gender, breed, mixed infections, and seasonal and spatial patterns. Veterinary Parasitology 136, 283295. pii: S0304-4017(05)00553-4; doi: 10.1016/j.vetpar.2005.11.012.
Garcia, H. H., Gonzalez, A. E., Gilman, R. H., Palacios, L. G., Jimenez, I., Rodriguez, S., Verastegui, M., Wilkins, P. and Tsang, V. C. (2001). Short report: transient antibody response in Taenia solium infection in field conditions – a major contributor to high seroprevalence. American Journal of Tropical Medicine and Hygiene 65, 3132.
Gawor, J., Borecka, A., Zarnowska, H., Marczynska, M. and Dobosz, S. (2008). Environmental and personal risk factors for toxocariasis in children with diagnosed disease in urban and rural areas of central Poland. Veterinary Parasitology 155, 217222. pii: S0304-4017(08)00266-5; doi: 10.1016/j.vetpar.2008.05.016.
Glickman, L. T. and Schantz, P. M. (1981). Epidemiology and pathogenesis of zoonotic toxocariasis. Epidemiologic Reviews 3, 230250.
Good, B., Holland, C. V., Taylor, M. R., Larragy, J., Moriarty, P. and O'Regan, M. (2004). Ocular toxocariasis in schoolchildren. Clinical Infectious Diseases 39, 173178. doi: 10.1086/421492; pii: CID32505.
Grimm, V., Berger, U., Bastiansen, F., Eliassen, S., Ginot, V., Giske, J., Goss-Custard, J., Grand, T., Heinz, S. K., Huse, G., Huth, A., Jepsen, J. U., Jørgensen, C., Mooij, W. M., Müller, B., Pe'er, G., Piou, C., Railsback, S. F., Robbins, A. M., Robbins, M. M., Rossmanith, E., Rüger, N., Strand, E., Souissi, S., Stillman, R. A., Vabø, R., Visser, U. and DeAngelis, D. L. (2006). A standard protocol for describing individual-based and agent-based models. Ecological Modelling 198, 115126. doi: 10.1016/j.ecolmodel.2006.04.023.
Grimm, V., Berger, U., DeAngelis, D. L., Polhill, J. G., Giske, J. and Railsback, S. F. (2010). The ODD protocol: a review and first update. Ecological Modelling 221, 27602768. doi: 10.1016/j.ecolmodel.2010.08.019.
Holland, C. V., O'Lorcain, P., Taylor, M. R. and Kelly, A. (1995). Sero-epidemiology of toxocariasis in school children. Parasitology 110, 535545.
Janeway, C. A. Jr. and Travers, P. (1997). Host defense against infection. In ImmunoBiology, The Immune System in Health and Disease. pp. 9-399-51. Current Biology Ltd London, UK; Garland Publishing, New York, USA.
Jansen, J., vanKnapen, F. Knapen, F., Schreurs, M. and vanWijngaarden, T. Wijngaarden, T. (1993). Toxocara ova in parks and sand-boxes in the city of Utrecht. Tijdschrift voor diergeneeskunde 118, 611614.
Jarosz, W., Mizgajska-Wiktor, H., Kirwan, P., Konarski, J., Rychlicki, W. and Wawrzyniak, G. (2010). Developmental age, physical fitness and Toxocara seroprevalence amongst lower-secondary students living in rural areas contaminated with Toxocara eggs. Parasitology 137, 5363. pii: S0031182009990874; doi: 10.1017/S0031182009990874.
Levin, S. (1999). Fragile Dominion: Complexity and the Commons. Perseus Books, Reading, MA, USA.
Liao, C. W., Sukati, H., D'Lamini, P., Chou, C. M., Liu, Y. H., Huang, Y. C., Chung, M. H., Mtsetfwa, J. S., Jonato, J., Chiu, W. T., Chang, P. W., Du, W. Y., Chan, H. C., Chu, T. B., Cheng, H. C., Su, W. W., Tu, C. C., Cheng, C. Y. and Fan, C. K. (2010). Seroprevalence of Toxocara canis infection among children in Swaziland, southern Africa. Annals of Tropical Medicine and Parasitology 104, 7380. doi: 10.1179/136485910X12607012373795.
Lopez, M. L., Martin, G., Chamorro, M. C. and Mario, A. J. (2005). Toxocariasis in children from a subtropical region. Medicina (B Aires) 65, 226230.
Magnaval, J. F., Michault, A., Calon, N. and Charlet, J. P. (1994). Epidemiology of human toxocariasis in La Reunion. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 531533.
Magnaval, J. F., Glickman, L. T., Dorchies, P. and Morassin, B. (2001). Highlights of human toxocariasis. Korean Journal of Parasitology 39, 111.
Martin, U. O. and Demonte, M. A. (2008). Urban contamination with zoonotic parasites in the central region of Argentina. Medicina (B Aires) 68, 363366.
Mizgajska, H. (2001). Eggs of Toxocara spp. in the environment and their public health implications. Journal of Helminthology 75, 147151. pii: S0022149X0100021X.
Mizgajska-Wiktor, H. and Uga, S. (2006). Exposure and environmental contamination. In Toxocara: The Enigmatic Parasite (ed. Holland, C. V. and Smith, H. V.), pp. 211227. CABI Publishing, Wallingford, UK.
Muradian, V., Gennari, S. M., Glickman, L. T. and Pinheiro, S. R. (2005). Epidemiological aspects of visceral larva migrans in children living at Sao Remo Community, Sao Paulo (SP), Brazil. Veterinary Parasitology 134, 9397. pii: S0304-4017(05)00317-1; doi: 10.1016/j.vetpar.2005.05.060.
Nagakura, K., Tachibana, H., Kaneda, Y. and Kato, Y. (1989). Toxocariasis possibly caused by ingesting raw chicken. Brazilian Journal of Infectious Diseases 160, 735736.
O'Lorcain, P. (1995). The effects of freezing on the viability of Toxocara canis and T. cati embryonated eggs. Journal of Helminthology 69, 169171.
Peel, M. C., Finlayson, B. L. and McMahon, T. A. (2007). Updated world map of the Köppen–Geiger climate classification. Hydrology and Earth System Sciences 11, 16331644.
Petzoldt, T. (2003). R as simulation platform in ecological modelling. R News 3, 816.
Pinelli, E., Herremans, T., Harms, M. G., Hoek, D. and Kortbeek, L. M. (2011). Toxocara and Ascaris seropositivity among patients suspected of visceral and ocular larva migrans in the Netherlands: trends from 1998 to 2009. European Journal of Clinical Microbiology and Infectious Diseases 30, 873879. doi: 10.1007/s10096-011-1170-9.
Radbruch, A., Muehlinghaus, G., Luger, E. O., Inamine, A., Smith, K. G., Dorner, T. and Hiepe, F. (2006). Competence and competition: the challenge of becoming a long-lived plasma cell. Nature Reviews. Immunology 6, 741750. pii: nri1886; doi: 10.1038/nri1886.
Radman, N. E., Archelli, S. M., Fonrouge, R. D., del V Guardis, M. and Linzitto, O. R. (2000). Human toxocarosis. Its seroprevalence in the city of La Plata. Memorias do Instituto Oswaldo Cruz 95, 281285. pii: S0074-02762000000300001.
R Development Core Team (2012). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Rinaldi, L., Biggeri, A., Carbone, S., Musella, V., Catelan, D., Veneziano, V. and Cringoli, G. (2006). Canine faecal contamination and parasitic risk in the city of Naples (southern Italy). BMC Veterinary Research 2, 29. pii: 1746-6148-2-29; doi: 10.1186/1746-6148-2-29.
Rubel, D. and Wisnivesky, C. (2005). Magnitude and distribution of canine fecal contamination and helminth eggs in two areas of different urban structure, Greater Buenos Aires, Argentina. Veterinary Parasitology 133, 339347. pii: S0304-4017(05)00299-2; doi: 10.1016/j.vetpar.2005.06.002.
Rubel, D., Zunino, G., Santillan, G. and Wisnivesky, C. (2003). Epidemiology of Toxocara canis in the dog population from two areas of different socioeconomic status, Greater Buenos Aires, Argentina. Veterinary Parasitology 115, 275286. pii: S0304401703001857.
Rubinsky-Elefant, G., da Silva-Nunes, M., Malafronte, R. S., Muniz, P. T. and Ferreira, M. U. (2008). Human toxocariasis in rural Brazilian Amazonia: seroprevalence, risk factors, and spatial distribution. American Journal of Tropical Medicine and Hygiene 79, 9398. pii: 79/1/93.
Rubinsky-Elefant, G., Hirata, C. E., Yamamoto, J. H. and Ferreira, M. U. (2010). Human toxocariasis: diagnosis, worldwide seroprevalences and clinical expression of the systemic and ocular forms. Annals of Tropical Medicine and Parasitology 104, 323. doi: 10.1179/136485910X12607012373957.
Santarem, V. A., Leli, F. N., Rubinsky-Elefant, G. and Giuffrida, R. (2011). Protective and risk factors for toxocariasis in children from two different social classes of Brazil. Revista do Instituto de Medicina Tropical de Sao Paulo 53, 6672. pii: S0036-46652011000200002.
Smith, H., Holland, C., Taylor, M., Magnaval, J. F., Schantz, P. and Maizels, R. (2009). How common is human toxocariasis? Towards standardizing our knowledge. Trends in Parasitology 25, 182188. pii: S1471-4922(09)00048-8; doi: 10.1016/
Soriano, S. V., Pierangeli, N. B., Roccia, I., Bergagna, H. F., Lazzarini, L. E., Celescinco, A., Saiz, M. S., Kossman, A., Contreras, P. A., Arias, C. and Basualdo, J. A. (2010). A wide diversity of zoonotic intestinal parasites infects urban and rural dogs in Neuquen, Patagonia, Argentina. Veterinary Parasitology 167, 8185. pii: S0304-4017(09)00600-1; doi: 10.1016/j.vetpar.2009.09.048.
Teixeira, C. R., Chieffi, P. P., Lescano, S. A., de Melo Silva, E. O., Fux, B. and Cury, M. C. (2006). Frequency and risk factors for toxocariasis in children from a pediatric outpatient center in southeastern Brazil. Revista do Instituto de Medicina Tropical de Sao Paulo 48, 251255. pii: S0036-46652006000500003.
Torgerson, P. R., Rosenheim, K., Tanner, I., Ziadinov, I., Grimm, F., Brunner, M., Shaiken, S., Shaikenov, B., Rysmukhambetova, A. and Deplazes, P. (2009). Echinococcosis, toxocarosis and toxoplasmosis screening in a rural community in eastern Kazakhstan. Tropical Medicine and International Health 14, 341348. pii: TMI2229; doi: 10.1111/j.1365–3156.2009.02229.x.
Uga, S., Minami, T. and Nagata, K. (1996). Defecation habits of cats and dogs and contamination by Toxocara eggs in public park sandpits. American Journal of Tropical Medicine and Hygiene 54, 122126.
Uga, S., Hoa, N. T., Noda, S., Moji, K., Cong, L., Aoki, Y., Rai, S. K. and Fujimaki, Y. (2009). Parasite egg contamination of vegetables from a suburban market in Hanoi, Vietnam. Nepal Medical College Journal 11, 7578.
Won, K. Y., Kruszon-Moran, D., Schantz, P. M. and Jones, J. L. (2008). National seroprevalence and risk factors for zoonotic Toxocara spp. infection. American Journal of Tropical Medicine and Hygiene 79, 552557. pii: 79/4/552.


Type Description Title
Supplementary materials

Kanobana supplementary material 1
Kanobana supplementary material 1

 Word (15 KB)
15 KB
Supplementary materials

Kanobana supplementary material 2
Kanobana supplementary material 2

 Word (13 KB)
13 KB


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed